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Receptor-mediated regional sympathetic nerve activation by leptin.
Open accessAbstract
Leptin is a peptide hormone produced by adipose tissue which acts centrally to decrease appetite and increase energy expenditure. Although leptin increases norepinephrine turnover in thermogenic tissues, the effects of leptin on directly measured sympathetic nerve activity to thermogenic and other tissues are not known. We examined the effects of intravenous leptin and vehicle on sympathetic nerve activity to brown adipose tissue, kidney, hindlimb, and adrenal gland in anesthetized Sprague-Dawley rats. Intravenous infusion of mouse leptin over 3 h (total dose 10-1,000 microg/kg) increased plasma concentrations of immunoreactive murine leptin up to 50-fold. Leptin slowly increased sympathetic nerve activity to brown adipose tissue (+286+/-64% at 1,000 microg/kg; P = 0.002). Surprisingly, leptin infusion also produced gradual increases in renal sympathetic nerve activity (+228+/-63% at 1,000 microg/kg; P = 0.0008). The effect of leptin on sympathetic nerve activity was dose dependent, with a threshold dose of 100 microg/kg. Leptin also increased sympathetic nerve activity to the hindlimb (+287+/-60%) and adrenal gland (388+/-171%). Despite the increase in overall sympathetic nerve activity, leptin did not increase arterial pressure or heart rate. Leptin did not change plasma glucose and insulin concentrations. Infusion of vehicle did not alter sympathetic nerve activity. Obese Zucker rats, known to possess a mutation in the gene for the leptin receptor, were resistant to the sympathoexcitatory effects of leptin, despite higher achieved plasma leptin concentrations. These data demonstrate that leptin increases thermogenic sympathetic nerve activity and reveal an unexpected stimulatory effect of leptin on overall sympathetic nerve traffic.
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In the citing paper
“These findings are in contrast to the effect of leptin administration on increase natriuresis (49, 50) and sympathetic activity (51) in normal, nonobese leptin-resistant Zucker rats (51).”
From The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men (2003) · cites this paper as [51]
Experimental — accuracy not yet measuredIn the citing paper
“Plasma leptin concentration is highly correlated with SNA activity123, and acute leptin infusions increase SNA in the brown adipose tissue, adrenal glands and kidneys of rodents124.”
From Obesity, kidney dysfunction and hypertension: mechanistic links (2019) · cites this paper as [124]
In the citing paper
“acute leptin administration in rodents increased SNS activity in brown adipose tissue (BAT), the adrenal gland, and the kidneys84.”
From Obesity-Induced Hypertension: Interaction of Neurohumoral and Renal Mechanisms (2015) · cites this paper as [84]
In the citing paper
“Acute leptin administration in rodents and humans increases renal and muscle SNS activity [45, 46] while chronic increases in plasma leptin levels, comparable to those found in severe obesity, caused sustained increases in BP and HR in rodents despite causing weight loss which would normally reduce BP [47].”
From Role of the brain melanocortins in blood pressure regulation (2017) · cites this paper as [45]
In the citing paper
“In addition its effects on appetite and metabolism, leptin acts in the brain to produce receptor-mediated increases in regional sympathetic activity91.”
From The Sympathetic Nervous System Alterations in Human Hypertension (2015) · cites this paper as [91]
In the citing paper
“Leptin is a potent appetite suppressant and, like insulin, stimulates the SNS.24,25”
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“Potential adverse effects of this hormone includes increased activity of the sympathetic nervous system and of the adrenal glands to secrete corticosteroids [7] and leptin thus not only increases metabolic rate but it also elevates blood pressure according to experimental studies [8-11].”
Sleep disordered breathing and risk factors for cardiovascular disease
Phillips, B. G., & Somers, V. K. (2002) · Current Opinion in Pulmonary Medicine · doi:10.1097/00063198-200211000-00006 · Cited by 37
Cold-induced alteration of adipokine profile in humans
Iwen, K. A., Wenzel, E., Ott, V., Perwitz, N., Wellhöner, P., Lehnert, H., Dodt, C., & Klein, J. C. (2010) · Metabolism · doi:10.1016/j.metabol.2010.03.011 · Cited by 36
Central Nervous System Dysfunction in Obesity-Induced Hypertension
Head, G. A., Lim, K., Barzel, B., Burke, S. L., & Davern, P. J. (2014) · Current Hypertension Reports · doi:10.1007/s11906-014-0466-4 · Cited by 37
Alamandine reduces leptin expression through the c-Src/p38 MAP kinase pathway in adipose tissue
Uchiyama, T., Okajima, F., Mogi, C., Tobo, A., Tomono, S., & Sato, K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0178769 · Cited by 36
Caloric restriction and mitochondrial function in the ageing myocardium
Rohrbach, S., Niemann, B., Abushouk, A. I., & Holtz, J. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.02.001 · Cited by 36
Leptin Increases Blood Pressure and Markers of Endothelial Activation during Pregnancy in Rats
Alshaikhli, H., Omar, E., Froemming, G. R. A., & Singh, H. J. (2013) · BioMed Research International · doi:10.1155/2013/298401 · Cited by 36
“Although the mechanism responsible for the rise in blood pressure following leptin treatment was not examined in this study, increases in blood pressure following leptin administration have been attributed to increases in sympathetic activity [24, 25], increased vasomotor activity and endothelial activation [26, 27],…”
BackgroundChemical sympathectomy alters regulation of body weight during prolonged ICV leptin infusion
Dobbins, R. L., Szczepaniak, L. S., Zhang, W., & McGarry, J. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00128.2002 · Cited by 38
“Sympathetic nerve terminals directly innervate brown and white adipose tissue and skeletal muscle (3–5, 26), and intravenous infusion of leptin has been shown to increase sympathetic nerve traffic to brown adipose tissue, kidney, adrenal medulla, and the hindlimb of rats (10, 21).”
BackgroundInsulin Resistance and Hypertension
Landsberg, L. (1999) · Clinical and Experimental Hypertension · doi:10.3109/10641969909061017 · Cited by 36
Factors Responsible for Obesity-Related Hypertension
Lim, K., Jackson, K. L., Sata, Y., & Head, G. A. (2017) · Current Hypertension Reports · doi:10.1007/s11906-017-0750-1 · Cited by 35
Tümer, N., Erdös, B., Matheny, M. E., Cudykier, I., & Scarpace, P. J. (2007) · Journal of Hypertension · doi:10.1097/hjh.0b013e3282e9a9fd · Cited by 35
Higher leptin is associated with hypertension: the Multi-Ethnic Study of Atherosclerosis
Allison, M., Ix, J. H., Morgan, C. L., McClelland, R. L., Rifkin, D. E., Shimbo, D., & Criqui, M. H. (2013) · Journal of Human Hypertension · doi:10.1038/jhh.2013.24 · Cited by 35
Leptin and the ventilatory response to exercise in heart failure
Wolk, R. A., Johnson, B. D., & Somers, V. K. (2003) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2003.06.007 · Cited by 35
Li, B., Shi, Z., Cassaglia, P. A., & Brooks, V. L. (2013) · Hypertension · doi:10.1161/hypertensionaha.111.00518 · Cited by 34
Miro, C., Cicatiello, A. G., Nappi, A., Sagliocchi, S., Acampora, L., Restolfer, F., Cuomo, O., de Alteriis, G., Pugliese, G., Torabinejad, S., et al. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.01.025 · Cited by 35
Sensitivity of ob/ob Mice to Leptin‐Induced Adipose Tissue Apoptosis
Della‐Fera, M. A., Choi, Y., Hartzell, D. L., Duan, J., Hamrick, M. W., & Baile, C. A. (2005) · Obesity Research · doi:10.1038/oby.2005.189 · Cited by 34
Hypertension and obstructive sleep apnea
Phillips, B. G., & Somers, V. K. (2003) · Current Hypertension Reports · doi:10.1007/s11906-003-0083-0 · Cited by 34
“Administration of leptin to animals results in increases in blood pressure [42] and in renal sympathetic nerve traffic [ 43 ].”
BackgroundCiriello, J., & Moreau, J. M. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00068.2012 · Cited by 33
Leptin increasing sympathetic nerve outflow in obesity
Simonds, S. E., Cowley, M. A., & Enriori, P. J. (2012) · Adipocyte · doi:10.4161/adip.20690 · Cited by 33
“Leptin has previously been demonstrated to have the ability to increase SNA in anaesthetised rats in a dose-dependent manner not only to BAT, but also to the adrenal, hind limb and kidney regions.(41) Overall, it is generally recognized that SNA is increased in obesity and, as we recently demonstrated, in BAT.”
BackgroundControl of respiratory and cardiovascular functions by leptin
Bassi, M., Furuya, W. I., Zoccal, D. B., Menani, J. V., Colombari, E., Hall, J. E., da Silva, A. A., do Carmo, J. M., & Colombari, D. S. A. (2015) · Life Sciences · doi:10.1016/j.lfs.2015.01.019 · Cited by 34
“administration of leptin increased SNA to the brown adipose tissue, kidneys and adrenal gland in lean rats [28,42].”
Effect of heart rate on the risk of developing metabolic syndrome
Inoue, T., Iseki, K., Iseki, C., Ohya, Y., Kinjo, K., & Takishita, S. (2009) · Hypertension Research · doi:10.1038/hr.2009.109 · Cited by 33
Leptin responses to glucose infusions in obesity-prone rats
Levy, J. R., Lesko, J. M., Krieg, R. J., Adler, R. A., & Stevens, W. D. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.5.e1088 · Cited by 33
“(18, 48) or by other mechanisms mediated by the autonomic nervous system (23).”
BackgroundAlshaikhli, H., Froemming, G. R. A., Omar, E., & Singh, H. J. (2014) · Reproductive Toxicology · doi:10.1016/j.reprotox.2014.08.006 · Cited by 33
Häfner, S., Baumert, J. J., Emeny, R. T., Lacruz, M. E., Thorand, B., Herder, C., Köenig, W., Rupprecht, R., & Ladwig, K. (2011) · Biological Psychology · doi:10.1016/j.biopsycho.2011.10.005 · Cited by 33
da Silva, A. A., Kuo, J. J., Tallam, L. S., Liu, J., & Hall, J. E. (2005) · Hypertension · doi:10.1161/01.hyp.0000198458.70351.e0 · Cited by 33
Lu, H., Buison, A. M., Jen, K. ‐. C., & Dunbar, J. C. (2000) · Peptides · doi:10.1016/s0196-9781(00)00301-6 · Cited by 33
The subcutaneous lipolytic response to regional neural stimulation is reduced in obese women.
Dodt, C., Lönnroth, P., Fehm, H., & Elam, M. (2000) · Diabetes · doi:10.2337/diabetes.49.11.1875 · Cited by 33
Leptin and blood pressure—is there a link?
Stenvinkel, P. (2000) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/15.8.1115 · Cited by 33
Loss of Leptin Actions in Obesity: Two Concepts with Cardiovascular Implications
Mark, A. L., Correia, M. L. G., Rahmouni, K., & Haynes, W. G. (2004) · Clinical and Experimental Hypertension · doi:10.1081/ceh-200031948 · Cited by 32
“Leptin increases sympathetic nerve activity to brown adipose tissue, the extremities and the kidney (13).”
BackgroundSelf-citationWatso, J. C., Fancher, I. S., Gomez, D. H., Hutchison, Z. J., Gutiérrez, O. M., & Robinson, A. T. (2023) · Obesity Reviews · doi:10.1111/obr.13589 · Cited by 42
Zhang, L., Liu, P.-F., Zhu, W., Cai, J., & Wang, Z. (2011) · Journal of Comparative Physiology B · doi:10.1007/s00360-011-0606-y · Cited by 32
Metadata
- Authors
- Haynes, W. G., Morgan, D. A., Walsh, S. A., Mark, A. L., & Sivitz, W. I.
- Affiliations
- University of Iowa (US)
- Venue
- Journal of Clinical Investigation
- Published
- 1997-07-15
- Volume
- 100
- Issue
- 2
- Pages
- 270-278
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC508189
- OpenAlex
- W2061340727
- Cited by
- 979
- References
- 29
- Citations by year
- 2026: 7 · 2025: 12 · 2024: 17 · 2023: 11 · 2022: 14 · 2021: 17 · 2020: 15 · 2019: 13 · 2018: 11 · 2017: 31 · 2016: 29 · 2015: 25 · 2014: 44 · 2013: 34 · 2012: 43
- FWCI
- 14.77
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs
- Wellcome Trust
- National Institutes of Health (5p50hl044546-05, 5r29hl043514-05)
- National Heart, Lung, and Blood Institute (HL-43514, HL-44546)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-25295, P30DK025295)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Keywords
- leptin, sympathetic activity, brown adipose tissue, renal sympathetic nerve activity, adrenal gland, thermogenesis, leptin receptor, Zucker fatty rats, norepinephrine, energy homeostasis
- MeSH terms
- Action Potentials, Adrenal Glands, Animals, Blood Glucose, Adipose Tissue, Brown, Disease Models, Animal, Hemodynamics, Hindlimb, Insulin, Kidney, Male, Obesity, Proteins, Rats, Zucker, Sympathetic Nervous System, Rats, Sprague-Dawley, Leptin, Rats
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